AJP spotted these Greater Painted-Snipe (Rostratula benghalensis) in Hong Kong last week. They were lurking at the edge of a reed bed. That’s a male in front—see the golden eyestripe—with a much more brightly coloured female almost hidden behind—see the white eyestripe. The species, found across South-East Asia, the Indian sub-continent and Africa, is polyandrous with the male incubating the eggs and rearing the young.
This sign board amongst the mangroves lining the Rio Cuero of the Cuero y Salada Wildlife Refuge in Honduras appears to have nothing goimg for it in the wildlife line. However, roosting in plain sight is a colony of Proboscis Bats (Rhynchonycteris naso). This bat goes by a variety of common names in the countries of Central and South America where it lives, often in wetlands: Brazilian Long-nosed Bat, Sharp-nosed Bat, River Bat and Long-nosed Proboscis Bat, the latter surely tautological. From the angle we viewed them it is not possible to see, because of foreshortening, the long nose.
This species is known to roost with the whole colony of 5-10 individuals lined up along branches, for example. It is small bat, around 6 cm long, nocturnal and insectivorous.
I was looking at old copies of Animal Life magazine, published in Britain in the early 1960s when I came across an article I remembered reading 62 years ago. It was by the French author and self-funded biologist Jean Rostand (1894-1977).
 |
| Animal Life No 2. October 1962 pp 34-38 |
Jean Rostand was wealthy enough to give up an ‘official’ career in science in order to continue research in his laboratory at home. Well known as a writer about science, the history of science and the human condition in the light of scientific discovery, much of his own research was on the development of amphibians from the egg. Some of his findings were overlooked, ignored or forgotten, only to be rediscovered decades later. He did achieve recognition in France, however, both scientific and literary.
In this article I will only consider one aspect of Rostand’s research: polydactyly in frogs and toads. He had found polydactyly of the hind limb (six toes in this case) in the Common Toad (Bufo bufo) and established it to be genetically determined. But then, in his own words:
...in a pond near Concarneau in Brittany I was surprised to find frogs with six, seven, eight and even nine toes. There was in fact a massive variation, affecting from ten to fifteen per cent of the population of the pond. Unlike the polydactyly of the toad, the polydactyly of the frog is not transmissible to its descendants: it is not, at any rate, transmitted in accordance with the accepted rules. It is simply the benign symptom of a much more serious anomaly which strikes the tadpole larvae and causes therein a considerable modification of the bone structure, the growth of supernumerary feet and the formation of various types of excrescence. All the tadpoles that are severely attacked perish before changing into frogs: the polydactylic adults are therefore survivors. What is the cause of this singular anomaly, which, in some respects, recalls certain malignant proliferations? Must one blame a physico-chemical factor, such as chemical substances or radiations, which are present in the surroundings? Or is it due to an infectious agent, a virus? The first hypothesis seems rather unlikely, because we know of no inorganic factor capable of producing such effects. If the second hypothesis can be proved—which is what I am trying to do at the moment—it is possible that the study of these abnormal larvae will throw some light on the formation mechanism of certain tumours. In any case the exhaustive study of anomalies, whether hereditary or acquired, among toads and frogs could, in one way or another, assist the study of human anomalies.
Rostand had in fact redescribed the syndrome. It had been first observed and reported in France in 1937.
Some observations were compatible with the variable presence of some agent. In some years ponds which had shown the anomaly in tadpoles were completely free of the condition but the cause remained unknown.
In 2017 Alain Dubois reviewed what was known and what was not known about Anomaly P. It has been found in a number of countries in Palaearctic water or green frogs, now separated off in their own genus, Pelophylax but not in frogs of the genus Rana. It may affect all species of Pelophylax including the kleptons between some of those species. The Edible Frog, Rana esculenta, now Pelophylax kl. esculentus, was the form studied by Rostand. Dubois wrote:
Much still remains to be known about the anomaly P: its cause, its geographic distribution, exactly which taxa are affected and why, what is the impact of this syndrome on frog populations, etc. Although this problem attracted the attention, especially of an amateur naturalist, Jean Rostand, mostly in the years 1950-1970, no studies are apparently under way nowadays, in any laboratory or European country, to elucidate these questions. This is surprising and even shocking, especially in view of the strong interest raised in recent years by amphibian anomalies in conservation biology.… Given the fact that this syndrome involves facts of cellular abnormal multiplication and tissue differentiation and growth, its understanding might throw interesting or important lights on some developmental biology problems. More attention should certainly be paid to this unsolved problem by the international scientific community.
But then things did start to happen. A group of Russian workers, later joined by the French, including Alain Dubois, found that Anomaly P is caused by the trematode Strigea robusta, i.e. a fluke. That work was mirrored by studies in North America which showed the devastating effects of trematode infection on some amphibian populations.
The life cycle of S. robusta involves three hosts: planorbid (ramshorn) snails as the first intermediate, then the larvae of amphibians as the second intermediate, with anatid birds (ducks, geese and swans) as the definitive host. An important clue was the occurrence of Anomaly P in water frog tadpoles when raised in tanks containing a species of planorbid snail.
Current evidence is that some amphibians are affected by S. robusta while others are not. In Russia the limbs of other amphibians that live alongside P. ribibundus, the Marsh Frog, and are infected show no abnormalities. Those unaffected are the Smooth Newt (Lissotriton vulgaris)(but see below), Great Crested Newt (Triturus cristatus), Pallas’s Spadefooi Toad (Pelobates vespertinus), Red-bellied Toad (Bombina bombina) and Moor Frog (Rana arvalis). However, there is evidence that when S. robusta appeared in a pond in Germany, the population of Smooth Newts (of which 73% were infected) declined. By contrast, there was no effect on the population of Great Crested Newts, none of which became infected. More recent work indicates that Anomaly P can be induced in toads (Common Toad, Bufo bufo; Green Toad, Bufotes viridis; Batura Toad, Bufotes baturae) by the presence of S. robusta.
Rostand’s experiments in the late 1940s and 50s indicated the existence of a sensitive period for during the early stages of a tadpole’s development for an infectious agent to act. This was confirmed with the experiments in which tadpoles were exposed to S. robusta. Once the toes had formed, the tadpole was safe. There was also evidence that the severe forms of Anomaly P depend on the stage of exposure, the parasite load, the location of the parasites and the degree of immunological protection.
Given the complex nature of the lifecycle of the parasite, variations in the populations of planorbid snails and ducks in a particular pond at a particular time it is perhaps not surprising that the occurrence of Anomaly P at a particular locale varies greatly in intensity.
The mechanism by which the trematode exerts its effect on the tadpole is beyond the scope of this article. However, research on trematode infection on development of the limb in North American amphibians suggested the production by the cercariae stage of the trematode of an excess of a Vitamin A metabolite which affects gene expression adversely.
There are, of course, unanswered questions, many on the ecological consequences of infection with the parasite. It also seems odd the parasite seems to be acting in a very unparasitical way—the selection pressure on parasites lies strongly against killing their hosts.
Rostand—the great ‘amateur’ developmental biologist—was right to conclude that the cause of Anomaly P is an infectious agent. However, it was not a virus but something much bigger, the fluke Strigea robusta.
 |
| From Svinin et al. 2020 |
 |
| From Svinin et al 2023 |
 |
| Jean Rostand Animal Life No 2. October 1962 |
Dubois A. 2017. Rostand’s anomaly P in Palaearctic green frogs (Pelophylax) and similar anomalies in amphibians. Mertensiella 25, 49-56
Svinin A, Bashinskiy I, Ermakov O, Litvinchuk S. 2023. Effects of minimum Strigea robusta (Digenea: Strigeidae) cercariae doses and localization of cystson the anomaly P manifestation in Pelophylax lessonae (Anura: Ranidae) tadpoles. Parasitology Research 122, 889-894. doi: 10.1007/s00436-022-07778-z
Svinin AO, Bashinskiy IV, Litvinchuk SN, Ermakov OA, Ivanov AY, Neymark LA, Vedernikov AA, Osipov VV, Drobot GP, Dubois A. 2020. Strigea robusta causes polydactylyand severe forms of Rostand’s anomaly P in water frogs. Parasites & Vectors 13, 381 doi.org/10.1186s13071-020-04256-2
Svinin AO, Chikhlyaev IV, Bashinskiy IW, Osipov VV, Neymark LA, Ivanov AY, Stoyko TG, Chernigova PI, Ibrogimova PK, Litvinchuk SN, Ermakov OA. 2023. Diversity of trematodes from the amphibian anomaly P hotspot: Role of planorbid snails. PLoS ONE 18(3): e0281740. doi.org/10.1371/journal.pone.0281740
Svinin A, Ermakov O, Litvinchuk S. 2022. The incidence of the anomaly P syndrome in water frogs (Anura, Ranidae, Pelophylax) from the Middle Volga River (Russia). Herpetozoa 35, 283–288 doi: 10.3897/herpetozoa.35.e95928
Svinin AO, Matushkina KA, Dedukh DV, Bashinskiy IV, Ermakov, OA, Litvinchuk SN. 2022. Strigea robusta (Digenea: Strigeidae) infection effects on the gonadal structure and limb malformation in toad early development. Journal of Experimental Zoology A 337, 675-686 doi.org/10.1002/jez.2599
Gangs of Montezuma Oropendolas are common in the grounds of the Lodge at Pico Bonito on the Caribbean side of Honduras. The colonial, woven hanging nests we saw at Lancetilla Botanical Gardens were unoccipied because were were not there in the breeding season. Then the males defend large harems of much smaller females and produce a complex warbling song, seemingly quite out of keeping with the size of the bird.
Relationships between the various species of oropendola appear to be contentious, probably unsurprising given the use of only mitochondrial DNA to form the basis of the statistical analysis. Psarocolius montezuma seems in common use along with Gymnostinops montezuma. It is found from Mexico to Panama.
2024, the centenary of the publication of Charles Elton’s classic paper, Periodic fluctuations in the numbers of animals: their causes and effects, in Journal of Experimental Biology, also saw a flurry of interest on the same topic and the same mammals that occupied a large part of Elton’s review, lemmings.
 |
| Norway Lemming, Lemmus lemmus Kevo Strict Nature Reserve, Finland, 2011 by Lakahillo (from Wikipedia) |
This is the authors’ summary:
Reports of fading vole and lemming population cycles and persisting low populations in some parts of the Arctic have raised concerns about the spread of these fundamental changes to tundra food web dynamics. By compiling 24 unique time series of lemming population fluctuations across the circumpolar region, we show that virtually all populations displayed alternating periods of cyclic/non-cyclic fluctuations over the past four decades. Cyclic patterns were detected 55% of the time (n = 649 years pooled across sites) with a median periodicity of 3.7 years, and non-cyclic periods were not more frequent in recent years. Overall, there was an indication for a negative effect of warm spells occurring during the snow onset period of the preceding year on lemming abundance. However, winter duration or early winter climatic conditions did not differ on average between cyclic and non-cyclic periods. Analysis of the time series shows that there is presently no Arctic-wide collapse of lemming cycles, even though cycles have been sporadic at most sites during the last decades. Although non-stationary dynamics appears a common feature of lemming populations also in the past, continued warming in early winter may decrease the frequency of periodic irruptions with negative consequences for tundra ecosystems.
Two commentaries were published on the paper by Charles Krebs and by Rudy Boonstra, well-known ecologists who work on population changes. These commentaries highlight the fact that despite decades of research the underlying cause of these population cycles in lemmings and other rodents remains unknown. Similarly, the physiological processes involved are also unknown. I have written previously on Dennis Chitty’s (1912-2010) attempts to identify the cause of population cycles in voles (see here).
What is clear is that the mathematical modelling approach pioneered by Alfred Lotka in 1925 based on changes in numbers of predators and prey over time and which have been pursued actively ever since are, as is so often the case with mathematical models, inadequate. Experimental approaches to lemming and vole cycles have also not, in general, been successful, with other possible explanations of any changes observed and doubt whether the experimental conditions imposed are ones that actually obtain in the wild.
The importance of trying to understand what happens under the snow—the habitat of lemmings in winter where they feed and breed—was also stressed in the commentaries. Those observing lemmings only see the results of that activity when they count the population in spring and summer.
It is easy to forget when discussing the cause of cyclicity in population size and the changes in reproductive rate necessary to drive such changes that the the occurrence of ‘lemming years’ is a major wildlife phenomenon. Elton wrote of the Norway Lemming, Lemmus lemmus:
For many years the lemmings have periodically forced themselves upon public attention in Southern Norway by migrating down in swarms into the lowland in autumn, and in many cases marching with great speed and determination into the sea, in attempting to swim across which they perish. The details of the fate of the migrants do not concern us here and are fully described by [R] Collett [1911-1912]….Lemming-years in Norway have the status of great floods or terrible winters.
and of lemmings in northern Scandinavia:
It is obvious that the phenomenon of migration is far more striking than a mere increase in the numbers. The spectacle of processions of lemmings ecstatically throwing themselves over the ends of railway bridges, and falling to an apparently useless death below; the sea strewn with dead lemmings like leaves on the ground after a storm; lemmings making a bee-line across crowded traffic oblivious to danger; all these things are bound to make people talk.
Is was descriptions like this that gave rise to the popular notion generated and churned by the news media that lemmings commit suicide rather than simply die en masse when presumably moving in large numbers in search of food (Elton wrote not of food but of ‘relieving congestion in an area’). The Walt Disney film White Wilderness (1958) showed the sort of scenes described by Elton and others, with lemmings tumbling over the edge of a cliff. Decades after I saw the film at a meeting of the school natural history society in 1960 it emerged that captured lemmings had been pushed over the edge of artificial rockwork. The footage may have been fake and the lemmings poorly treated but film certainly conveyed what happens in the wild.
There are questions in my mind on this related phenomenon of migration, like the distances involved and whether they are acting like a plague of locusts, stripping one area of food before having to move on, given that their body size and increased activity would suggest they would starve to death within a week without food. However, it is the response to overcrowding view that dominated research in this area for decades. But that is another story.
To conclude, 100 years after Elton, the cause(s) and mechanism(s) of population cycles in lemmings—and voles etc—remain unsolved. But research activity and monitoring continues. We can only hope for progress.
- - - - - - - - - - - - - - - - - - - - -
As an afternote I found reading Elton’s paper from 1924 well worth while. Not only did he consider mechanisms that may account for the phenomenon in lemmings but he also reviewed the occurrence of periodic booms in population of other rodents in some years. In the garden we had a large population of Bank Voles in the summers of 2018 and 2019, but not in the years before or since. Are the same or different mechanisms at play in different species is another abiding question.
Boonstra R. 2024. Population regulation and limitation—insights from lemming cycles: past, present and future. Proceedings of the Royal Society B 291: 20240660. doi.org/10.1098/rspb.2024.0660
Elton CS. 1924. Periodic fluctuations in the numbers of animals: their causes and effects. Journal of Experimental Biology 2, 119–163. doi.org/10.1242/jeb.2.1.119
Gauthier G, Ehrich D, Belke-Brea M, Domine F, Alisauskas R, Clark K, Ecke F, Eide NE, Framstad E, Frandsen J, Gilg O, Henttonen H, Hörnfeldt B, Kataev GD, Menyushina IE, Oksanen L, Oksanen T, Olofsson J, Samelius G, Sittler B, Smith PA, Sokolov AA, Sokolova NA, Schmidt NM. 2024. Taking the beat of the Arctic: are lemming population cycles changing due to winter climate? Proceedings of the Royal Society B 291: 20232361. doi.org/10.1098/rspb.2023.2361
Krebs CJ. 2024. Lemming population fluctuations around the Arctic. Proceedings of the Royal Society B 291: 20240399. doi: 10.1098/rspb.2024.0399
We saw the Central American Agouti (Dasyprocta punctata) several times while walking in the gardens of the Lodge at Pico Bonito in Honduras. These hystricomorph rodents are diurnal and live as mongamous pairs. Most times we saw one it was carrying one of these large seed pods.
After my article on the artist Commander Alfred Marcus Hughes appeared, Greg Davies commented:
Hughes also makes a cameo appearance in Beryl Patricia Hall's autobiography "A Hawk from a Handsaw" (1993). Hall was the doyenne of the British Museum Bird Room in the post-war III period, and a relative of Hughes.
On looking up Hughes and Hall I found that they were first cousins, once removed. Pat Hall was the grand-daughter of Hughes’s mother’s brother.
The comment also rang a bell in my neural circuitry. I was sure I could remember meeting Pat Hall but could not recall where and how. Then, looking her up to write this article, I found a photograph which provided all the answers. The date was 4 May 1972 when she received the Stamford Raffles Award at the AGM of the Zoological Society of London. I remember speaking to her briefly after the meeting when she seemed a bundle of nerves. For some strange reason on seeing the photograph I immediately remembered the coat she was wearing as being several sizes too big such that she and the coat seemed moved independently—a very weird thing to recall from the memory bank after 52 years.
 |
| Pat Hall receiving the Stamford Raffles Award from the President of the Zoological Society of London, Prince Philip, Duke of Edinburgh. 4 May 1972 (Annual Report for 1972, ZSL) |
Pat Hall was Beryl Patricia Hall (née Woodhouse). She was born to a wealthy family in Epson, Surrey, in 1917. She was thwarted by her parents in going to Cambridge to study maths and instead spent four years at home kicking her heels but also developing an interest in birdwatching. Thus in the 1939 Register, the emergency census, she is shown as employed on ‘domestic duties’ but also as involved in Air Raid Precautions work teaching ambulance drivers. She was determined to do something for the war effort and joined the Mechanised Transport Corps, a uniformed women’s civilian organisation that provided drivers to government departments and other civilian services.
After the outbreak of war Pat Hall became engaged to John Clavell Hall, in civilian life a Winchester-educated insurance clerk. He was commissioned into the Royal Artillery in March 1940 and posted to the Middle East. Pat volunteered to serve overseas driving ambulances. She was first in South Africa but was then moved to Egypt. The two were married on 21 May 1941 at Suez. However, this was no happily-ever-after story. By June 1943 John Hall had fought in Crete. was a temporary Captain and had been mentioned in despatches. However later that year he was captured during the Battle of Leros in the Dodecanese Campaign. Pat further developed her interest in birds in North Africa and ended the war in Italy still driving ambulances. After the war the marriage broke down and it was then that Hughes must have offered his help.
Alfred Hughes was a friend of the Norman Boyd Kinnear of the Natural History Museum. Kinnear, with no academic qualifications, had risen through the ranks of the museum world, beginning at the Bombay Natural History Society’s museum in Calcutta and continuing at the Natural History Museum in London. He had specialised in ornithology. By the time the war was ending he had been appointed Keeper of Zoology. In 1947 he was asked to take over as Director, past the normal retirement age, until a suitable candidate had been found in the post-war world. He stayed on as Director until 1950, sorting out the repair and restoration of the Museum needed after the disruption and damage caused by the War; for this he received a ‘K’.
Through that contact with Kinnear, Pat Hall was offered a post of Associate Scientific Worker in the Bird Room of the Museum. Ideally suited for those wealthy enough not needing to find paid employment, the scheme provided cheap and enthusiastic voluntary labour to the Museum. The position was paid at a rate—which did not change for ten years—of four shillings per hour, a wage which would have exceeded the average industrial pay in the 1940s. However, instead of that equating to a salary of around £800 per year, the maximum pay each year was capped at £100. Pat Hall was clearly keen to work at the Museum; she turned down a job offer from the BBC in order to work at the Museum.
James David Macdonald (1908-2002) was in charge of the Bird Room. He recognised her aptitude for the work she was doing and given her experience in Africa and her skills as a motor mechanic invited her, at her own expense, to be a member of a collecting expedition to south-west Africa that began in late 1949. The team, including Macdonald’s wife as the team doctor and cook, collected 1300 specimens of nearly 200 species during the six months in the field. After that for nearly 20 years Pat Hall divided her time between curatorial work, collecting expeditions and research based on the collections in the Museum. Her expeditions during the 1950s were to Africa. In 1953 she organised and largely funded a Natural History Museum-backed trip to what is now Botswana. Before and after an ornithological congress in Livingstone in what is now Zambia, she collected in Botswana and Angola respectively; overall she collected around 2000 specimens for the Museum. A short trip to north-western Botswana was her final experience of collecting in Africa.
Her publications during the 1950s and 60s were on African birds. Her largest was the outcome of eight years of work: An Atlas of Speciation in African Passerine Birds in 1970. Of 423 pages with 439 maps it was widely praised by reviewers. Herbert Friedmann (1900-1987) the American ornithologist who worked at the Smithsonian Institution wrote of its importance in The Auk of July 1971:
As Mrs. Hall states at the beginning of her introduction, this great series of maps constitutes the first attempt to show in graphic form, for the ready comprehension of the student, the results, "and the continuing process, of evolution in a large continental avifauna by means of plotting on one map the distribution of species believed to be immediately descended from a common ancestor." By placing closely related species on the same map it becomes evident where they overlap and where the are allopatric, and these facts give the field student indications of where to look and what to study in an attempt to assess and to interpret the past history of each of these current distributional patterns. It must be kept in mind, when using this atlas, that every existing specific distributional picture is not merely a discrete fact of local interest, but is always, and inevitably, the result of the past history of the species and of the region. This is the real, inherent interest in each of them, and each could become a valid point of departure for further study of the evolutionary vicissitudes of the particular species.
The Atlas had started as a joint effort with Reginald Ernest Moreau (1897–1970) the great amateur scientific ornithologist of his day. However, he became increasingly ill and the work fell on Mrs Hall. He died in the year of its publication.
Work on African birds was interrupted in the early 1960s. Macdonald heard of and then approached Harold Hall (no relation to Pat) an Australian philanthropist who was interested in supporting research. Harold Hall agreed to sponsor a series of five expeditions for the Natural History Museum (still labouring under the title of British Museum (Natural History)) around Australia. Macdonald was very keen to obtain more specimens for the Museum. The number of Australian specimens available within Britain had been depleted by the sale of Lord Rothschild’s collection (Rothschild was being blackmailed by a ‘titled lady’ and he needed the money) and another private collection to the USA.
Pat Hall led the third Harold Hall Expedition given her experience of collecting in arid parts of Africa. That was to the interior of Western and South Australia. She then edited the book describing the findings of all five expeditions which was published in 1974.
After the post-war recovery the Natural History Museum on its site in London was bursting at the seams with many thousands of specimens stored in unsuitable accommodation. In the mid-1960s, plans emerged to move the bird collection from South Kensington to the site of the Rothschild Museum at Tring in Hertfordshire. Pat Hall was opposed to the move on scientific grounds. It is easy to see why. She would also have had to move from Surrey to somewhere nearer Tring. She therefore decided to give up her work at the Museum in 1971. At the same time she moved from Epsom to the New Forest in Hampshire where it was noted she devoted her time ‘to friends, dogs, horses and village life’. However, retirement from the ornithological world in which she was well known came more gradually. She was in demand as an editor, speaker and organiser. What appears to have been her last job was presidency of the 4th Pan-African Ornithological Congress in 1976. That caused her particular hassles because of its move at the last minute from Kenya to the Seychelles over political problems.
It was said that the award which gave her particular pleasure was the Stamford Raffles Award of the Zoological Society of London for 1971—presented by the Society’s President, Prince Philip, Duke of Edinburgh at the Annual General Meeting I attended in 1972. This is how the Annual Report recorded it:
The Stamford Raffles Award (awarded to an amateur zoologist for distinguished contributions to zoology) to Mrs B. P. Hall, British Museum (Natural History), in recognition of her work on the taxonomy and zoogeography of birds, particularly those of Africa. The award was a sculpture in bronze, Wild Boar, by Miss Elisabeth Frink.
It was though the final paragraph of citation for the Union Medal of the British Ornithologists’ Union that best sums up what she had achieved:
Her scientific work has already been widely recognised, by her election as Corresponding Fellow of the American Ornithologists' Union, and by the awards of the Gill Memorial Medal of the South African Ornithological Society and the Stamford Raffles Award of the Zoological Society of London. It is most fitting that the Union Medal should now be awarded to Pat Hall, who has so strikingly shown that the heights of ornithological achievement can still be scaled without the benefit of formal academic qualifications and institutional backing.
I wonder if Alfred Hughes realised that in speaking to his friend Kinnear he was launching his cousin Pat Hall on a pathway to her becoming a major player in classical ornithology of the 20th century. The Hughes-Hall family axis runs wide and deep in the ornithology of Africa and Asia.
Beryl Patricia Hall died on 4 August 2010 in a nursing home at Fishbourne, Hampshire.
Prys-Jones R. 2011. Beryl Patricia Hall (née Woodhouse), 1917-2010. Ibis 153, 913-914.
